Epigenetics as Driver of Adaptation and Diversification in Microbial Eukaryotes

Weiner, Agnes; Katz, Laura A.

doi:10.3389/fgene.2021.642220

Cited by 20 publications

(19 citation statements)

References 76 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…McGrath & Katz 2004 [1] ; Weiner & Katz 2021 [81] ), though two manuscripts also address variability within prokaryotes and at the origin of eukaryotes (Collens & Katz 2021 [79] ; Oliverio & Katz 2014 [2] ). Below we exemplify just a few of these life cycle variants.…”

Section: Box 1: Foraminifera Are Just One Example Of the Diversity Of...mentioning

confidence: 99%

Foraminifera as a model of the extensive variability in genome dynamics among eukaryotes

et al. 2022

Self Cite

View full text Add to dashboard Cite

Knowledge of eukaryotic life cycles and associated genome dynamics stems largely from research on animals, plants, and a small number of "model" (i.e., easily cultivable) lineages. This skewed sampling results in an underappreciation of the variability among the many microeukaryotic lineages, which represent the bulk of eukaryotic biodiversity. The range of complex nuclear transformations that exists within lineages of microbial eukaryotes challenges the textbook understanding of genome and nuclear cycles. Here, we look in-depth at Foraminifera, an ancient (∼600 million-year-old) lineage widely studied as proxies in paleoceanography and environmental biomonitoring.We demonstrate that Foraminifera challenge the "rules" of life cycles developed largely from studies of plants and animals. To this end, we synthesize data on foraminiferal life cycles, focusing on extensive endoreplication within individuals (i.e., single cells), the unusual nuclear process called Zerfall, and the separation of germline and somatic function into distinct nuclei (i.e., heterokaryosis). These processes highlight complexities within lineages and expand our understanding of the dynamics of eukaryotic genomes.

show abstract

Section: Box 1: Foraminifera Are Just One Example Of the Diversity Of...mentioning

confidence: 99%

Foraminifera as a model of the extensive variability in genome dynamics among eukaryotes

et al. 2022

Self Cite

View full text Add to dashboard Cite

show abstract

“…Previous studies suggest that genomic organizational patterns may serve as mechanisms for rapid reproductive incompatibility between ciliates (Collens & Katz, 2021; Gao et al, 2014, 2015; Nowacki et al, 2011; Weiner & Katz, 2021). We consider this concept in our analyses of the micronuclear genome and macronuclear transcriptome of S. arcuata and S. meunieri , which reveal different patterns of micronuclear organization, including the gene regions presented in Figure 8, which are >98% identical in the MAC of both ciliates (Table S1).…”

Section: Discussionmentioning

confidence: 99%

“…In particular, single-cell transcriptomics and genomics (single-cell 'omics) allow for the comparison of germline micronuclear and somatic macronuclear loci, which can reveal complex patterns of genome rearrangement (Maurer-Alcalá et al, 2018). These patterns represent a heritable genomic distinction (Nowacki et al, 2011) and an epigenetic driver of diversification (Weiner & Katz, 2021) that may help to discriminate genetically isolated species. Genome rearrangements occur between the germline micronucleus (MIC) and the transcriptionally active somatic macronucleus (MAC) following conjugation, when the zygotic nucleus divides and differentiates into a new MIC and MAC.…”

Section: Introductionmentioning

confidence: 99%

Genome architecture used to supplement species delineation in two cryptic marine ciliates

Smith

Santoferrara

Katz

et al. 2022

Molecular Ecology Resources

Self Cite

View full text Add to dashboard Cite

The purpose of this study is to determine which taxonomic methods can elucidate clear and quantifiable differences between two cryptic ciliate species, and to test the utility of genome architecture as a new diagnostic character in the discrimination of otherwise indistinguishable taxa. Two cryptic tintinnid ciliates, Schmidingerella arcuata and Schmidingerella meunieri, are compared via traditional taxonomic characters including lorica morphometrics, ribosomal RNA (rRNA) gene barcodes and ecophysiological traits. In addition, single‐cell ‘omics analyses (single‐cell transcriptomics and genomics) are used to elucidate and compare patterns of micronuclear genome architecture between the congeners. The results include a highly similar lorica that is larger in S. meunieri, a 0%–0.5% difference in rRNA gene barcodes, two different and nine indistinguishable growth responses among 11 prey treatments, and distinct patterns of micronuclear genomic architecture for genes detected in both ciliates. Together, these results indicate that while minor differences exist between S. arcuata and S. meunieri in common indices of taxonomic identification (i.e., lorica morphology, DNA barcode sequences and ecophysiology), differences exist in their genomic architecture, which suggests potential genetic incompatibility. Different patterns of micronuclear architecture in genes shared by both isolates also enable the design of species‐specific primers, which are used in this study as unique “architectural barcodes” to demonstrate the co‐occurrence of both ciliates in samples collected from a NW Atlantic estuary. These results support the utility of genomic architecture as a tool in species delineation, especially in ciliates that are cryptic or otherwise difficult to differentiate using traditional methods of identification.

show abstract

“…Mostly, they reproduce asexually, and, therefore, it remains enigmatic how the enormous diversity of protists was generated. Weiner and Katz argued that epigenetic processes such as chromatin modification and regulation by small non-coding RNAs that can rapidly modify genomes and gene expression states play important roles in driving phenotypic plasticity, differential adaptation and perhaps speciation of protists [ 126 ].…”

Section: Environmental Adaptation Of Clonal Organisms With the Help O...mentioning

confidence: 99%

Environmental Adaptation of Genetically Uniform Organisms with the Help of Epigenetic Mechanisms—An Insightful Perspective on Ecoepigenetics

Vogt

2022

Epigenomes

View full text Add to dashboard Cite

Organisms adapt to different environments by selection of the most suitable phenotypes from the standing genetic variation or by phenotypic plasticity, the ability of single genotypes to produce different phenotypes in different environments. Because of near genetic identity, asexually reproducing populations are particularly suitable for the investigation of the potential and molecular underpinning of the latter alternative in depth. Recent analyses on the whole-genome scale of differently adapted clonal animals and plants demonstrated that epigenetic mechanisms such as DNA methylation, histone modifications and non-coding RNAs are among the molecular pathways supporting phenotypic plasticity and that epigenetic variation is used to stably adapt to different environments. Case studies revealed habitat-specific epigenetic fingerprints that were maintained over subsequent years pointing at the existence of epigenetic ecotypes. Environmentally induced epimutations and corresponding gene expression changes provide an ideal means for fast and directional adaptation to changing or new conditions, because they can synchronously alter phenotypes in many population members. Because microorganisms inclusive of human pathogens also exploit epigenetically mediated phenotypic variation for environmental adaptation, this phenomenon is considered a universal biological principle. The production of different phenotypes from the same DNA sequence in response to environmental cues by epigenetic mechanisms also provides a mechanistic explanation for the “general-purpose genotype hypothesis” and the “genetic paradox of invasions”.

show abstract

Epigenetics as Driver of Adaptation and Diversification in Microbial Eukaryotes

Cited by 20 publications

References 76 publications

Foraminifera as a model of the extensive variability in genome dynamics among eukaryotes

Foraminifera as a model of the extensive variability in genome dynamics among eukaryotes

Genome architecture used to supplement species delineation in two cryptic marine ciliates

Environmental Adaptation of Genetically Uniform Organisms with the Help of Epigenetic Mechanisms—An Insightful Perspective on Ecoepigenetics

Contact Info

Product

Resources

About